{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,28]],"date-time":"2026-09-28T17:00:33Z","timestamp":1790614833966,"version":"4.1.0"},"reference-count":22,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2019,9,18]],"date-time":"2019-09-18T00:00:00Z","timestamp":1568764800000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2019,9,18]],"date-time":"2019-09-18T00:00:00Z","timestamp":1568764800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100004440","name":"Wellcome Trust","doi-asserted-by":"publisher","award":["203919\/Z\/16\/Z"],"award-info":[{"award-number":["203919\/Z\/16\/Z"]}],"id":[{"id":"10.13039\/100004440","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000268","name":"Biotechnology and Biological Sciences Research Council","doi-asserted-by":"publisher","award":["BB\/1015655\/1"],"award-info":[{"award-number":["BB\/1015655\/1"]}],"id":[{"id":"10.13039\/501100000268","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["BMC Vet Res"],"published-print":{"date-parts":[[2019,12]]},"abstract":"Abstract<\/jats:title>\n \n Background<\/jats:title>\n \n Dogs that have clinical leishmaniosis (ClinL), caused by the parasite\n Leishmania infantum<\/jats:italic>\n , are commonly co-infected with other pathogens, especially vector-borne pathogens (VBP). A recent PCR-based study found that ClinL dogs are more likely to be additionally infected with the rickettsial bacteria\n Ehrlichia canis<\/jats:italic>\n . Further information on co-infections in ClinL cases with VBP, as assessed by serology, is required. The research described in this report determined if dogs with ClinL are at higher risk of exposure to VBP than healthy control dogs using a case-control serology study.\n <\/jats:p>\n <\/jats:sec>\n \n Results<\/jats:title>\n \n Of the 47 dogs with ClinL, anti-\n E. canis<\/jats:italic>\n \/\n Ehrlichia ewingii<\/jats:italic>\n antibodies were detected in 17 (36.2%), anti-\n Anaplasma phagocytophilum<\/jats:italic>\n \/\n Anaplasma platys<\/jats:italic>\n antibodies in 5 (10.6%) and antigen for\n Dirofilaria immitis<\/jats:italic>\n in 2 (4.3%). Of the 87 control dogs, anti-\n E. canis<\/jats:italic>\n \/\n E<\/jats:italic>\n .\n ewingii<\/jats:italic>\n antibodies were detected in 14 (16.1%) and anti-\n A<\/jats:italic>\n .\n phagocytophilum<\/jats:italic>\n \/\n A<\/jats:italic>\n .\n platys<\/jats:italic>\n antibodies in 2 (2.3%). No anti-\n Borrelia burgdorferi<\/jats:italic>\n antibody tests were positive. No statistical differences between the ClinL dogs and control dogs regarding lifestyle or use of ectoparasitic prevention, were identified. The ClinL was significantly associated with anti-\n E. canis<\/jats:italic>\n \/\n E<\/jats:italic>\n .\n ewingii<\/jats:italic>\n antibodies (odds ratio\u2009=\u20092.9, 95% confidence interval: 1.3\u20136.7,\n P<\/jats:italic>\n \u2009=\u20090.010) compared to controls by both multivariable logistic regression and structural equation modelling.\n <\/jats:p>\n <\/jats:sec>\n \n Conclusions<\/jats:title>\n \n It was demonstrated that an increased risk for\n E. canis<\/jats:italic>\n \/\n E<\/jats:italic>\n .\n ewingii<\/jats:italic>\n seropositivity is present in dogs with ClinL compared to clinically healthy control dogs, despite similar ectoparasitic prevention use and lifestyle. Based on these findings it is suggested that dogs with ClinL should not only be tested for\n E. canis<\/jats:italic>\n co-infection using PCR but also serologically for\n E. canis<\/jats:italic>\n \/\n E<\/jats:italic>\n .\n ewingii<\/jats:italic>\n .\n <\/jats:p>\n <\/jats:sec>","DOI":"10.1186\/s12917-019-2083-6","type":"journal-article","created":{"date-parts":[[2019,9,18]],"date-time":"2019-09-18T07:05:02Z","timestamp":1568790302000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":20,"title":["Associations between clinical canine leishmaniosis and multiple vector-borne co-infections: a case-control serological study"],"prefix":"10.1186","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-6039-6586","authenticated-orcid":false,"given":"Charalampos","family":"Attipa","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laia","family":"Solano-Gallego","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christian M.","family":"Leutenegger","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kostas","family":"Papasouliotis","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Francesca","family":"Soutter","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"J\u00f6rg","family":"Balzer","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Scott","family":"Carver","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jesse S.","family":"Buch","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"S\u00e9verine","family":"Tasker","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2019,9,18]]},"reference":[{"issue":"3","key":"2083_CR1","doi-asserted-by":"publisher","first-page":"279","DOI":"10.1016\/S0738-081X(99)00046-2","volume":"17","author":"R Killick-Kendrick","year":"1999","unstructured":"Killick-Kendrick R. The biology and control of Phlebotomine sand flies. Clin Dermatol. 1999;17(3):279\u201389.","journal-title":"Clin Dermatol"},{"issue":"4","key":"2083_CR2","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1016\/j.pt.2009.01.003","volume":"25","author":"D Otranto","year":"2009","unstructured":"Otranto D, Dantas-Torres F, Breitschwerdt EB. Managing canine vector-borne diseases of zoonotic concern: part one. Trends Parasitol. 2009;25(4):157\u201363.","journal-title":"Trends Parasitol"},{"issue":"1","key":"2083_CR3","doi-asserted-by":"publisher","first-page":"97","DOI":"10.1186\/1756-3305-6-97","volume":"6","author":"AS De Tommasi","year":"2013","unstructured":"De Tommasi AS, Otranto D, Dantas-Torres F, Capelli G, Breitschwerdt EB, de Caprariis D. Are vector-borne pathogen co-infections complicating the clinical presentation in dogs? Parasit Vectors. 2013;6(1):97.","journal-title":"Parasit Vectors"},{"key":"2083_CR4","doi-asserted-by":"publisher","first-page":"48","DOI":"10.1186\/1756-3305-4-48","volume":"4","author":"MJ Day","year":"2011","unstructured":"Day MJ. The immunopathology of canine vector-borne diseases. Parasit Vectors. 2011;4:48.","journal-title":"Parasit Vectors"},{"issue":"1","key":"2083_CR5","doi-asserted-by":"publisher","first-page":"135","DOI":"10.1186\/s13071-018-2724-9","volume":"11","author":"M Baxarias","year":"2018","unstructured":"Baxarias M, \u00c1lvarez-Fern\u00e1ndez A, Mart\u00ednez-Orellana P, Montserrat-Sangr\u00e0 S, Ordeix L, Rojas A, et al. Does co-infection with vector-borne pathogens play a role in clinical canine leishmaniosis? Parasit Vectors. 2018;11(1):135.","journal-title":"Parasit Vectors"},{"issue":"1","key":"2083_CR6","doi-asserted-by":"publisher","first-page":"184","DOI":"10.1186\/s13071-018-2717-8","volume":"11","author":"C Attipa","year":"2018","unstructured":"Attipa C, Solano-Gallego L, Papasouliotis K, Soutter F, Morris D, Helps C, et al. Association between canine leishmaniosis and Ehrlichia canis co-infection: a prospective case-control study. Parasit Vectors. 2018;11(1):184.","journal-title":"Parasit Vectors"},{"issue":"Suppl 2","key":"2083_CR7","doi-asserted-by":"publisher","first-page":"30","DOI":"10.1111\/j.1469-0691.2008.02150.x","volume":"15","author":"Y Mekuzas","year":"2009","unstructured":"Mekuzas Y, Gradoni L, Oliva G, Foglia Manzillo V, Baneth G. Ehrlichia canis and Leishmania infantum co-infection: a 3-year longitudinal study in naturally exposed dogs. Clin Microbiol Infect. 2009;15(Suppl 2):30\u20131.","journal-title":"Clin Microbiol Infect"},{"issue":"2","key":"2083_CR8","doi-asserted-by":"publisher","first-page":"231","DOI":"10.1051\/vetres:2005054","volume":"37","author":"L Solano-Gallego","year":"2006","unstructured":"Solano-Gallego L, Llull J, Osso M, Hegarty B, Breitschwerdt E. A serological study of exposure to arthropod-borne pathogens in dogs from northeastern Spain. Vet Res. 2006;37(2):231\u201344.","journal-title":"Vet Res"},{"issue":"Suppl 1","key":"2083_CR9","doi-asserted-by":"publisher","first-page":"S101","DOI":"10.1007\/s00436-009-1501-2","volume":"105","author":"N Pantchev","year":"2009","unstructured":"Pantchev N, Schaper R, Limousin S, Norden N, Weise M, Lorentzen L. Occurrence of Dirofilaria immitis and tick-borne infections caused by Anaplasma phagocytophilum, Borrelia burgdorferi sensu lato and Ehrlichia canis in domestic dogs in France: results of a countrywide serologic survey. Parasitol Res. 2009;105(Suppl 1):S101\u201314.","journal-title":"Parasitol Res"},{"key":"2083_CR10","doi-asserted-by":"publisher","first-page":"117","DOI":"10.1186\/1756-3305-6-117","volume":"6","author":"G Mir\u00f3","year":"2013","unstructured":"Mir\u00f3 G, Montoya A, Roura X, G\u00e1lvez R, Sainz A. Seropositivity rates for agents of canine vector-borne diseases in Spain: a multicentre study. Parasit Vectors. 2013;6:117.","journal-title":"Parasit Vectors"},{"issue":"9","key":"2083_CR11","doi-asserted-by":"publisher","first-page":"3506","DOI":"10.1128\/JCM.40.9.3506-3508.2002","volume":"40","author":"M B\u00e9langer","year":"2002","unstructured":"B\u00e9langer M, Sorenson HL, France MK, Bowie MV, Barbet AF, Breitschwerdt EB, et al. Comparison of serological detection methods for diagnosis of Ehrlichia canis infections in dogs. J Clin Microbiol. 2002;40(9):3506\u20138.","journal-title":"J Clin Microbiol"},{"issue":"4","key":"2083_CR12","doi-asserted-by":"publisher","first-page":"523","DOI":"10.1007\/s10493-016-0091-9","volume":"70","author":"A Tsatsaris","year":"2016","unstructured":"Tsatsaris A, Chochlakis D, Papadopoulos B, Petsa A, Georgalis L, Angelakis E, et al. Species composition, distribution, ecological preference and host association of ticks in Cyprus. Exp Appl Acarol. 2016;70(4):523\u201342.","journal-title":"Exp Appl Acarol"},{"key":"2083_CR13","first-page":"100330","volume":"18","author":"P Kokkinos","year":"2019","unstructured":"Kokkinos P, Dimzas D, Pantchev N, Tamvakis A, Balzer J, Diakou A. Filarial infections in dogs in Cyprus, an apparently heartworm free island. Vet Parasitol. 2019;18:100330.","journal-title":"Vet Parasitol"},{"issue":"3","key":"2083_CR14","doi-asserted-by":"publisher","first-page":"441","DOI":"10.4269\/ajtmh.2010.09-0282","volume":"82","author":"A Mazeris","year":"2010","unstructured":"Mazeris A, Soteriadou K, Dedet JP, Haralambous C, Tsatsaris A, Moschandreas J, et al. Leishmaniases and the Cyprus paradox. Am J Trop Med Hyg. 2010;82(3):441\u20138.","journal-title":"Am J Trop Med Hyg"},{"issue":"3","key":"2083_CR15","doi-asserted-by":"publisher","first-page":"341","DOI":"10.1016\/j.ttbdis.2016.12.006","volume":"8","author":"C Attipa","year":"2017","unstructured":"Attipa C, Hicks CA, Barker EN, Christodoulou V, Neofytou K, Mylonakis ME, et al. Canine tick-borne pathogens in Cyprus and a unique canine case of multiple co-infections. Ticks Tick-Borne Dis. 2017;8(3):341\u20136.","journal-title":"Ticks Tick-Borne Dis"},{"issue":"6","key":"2083_CR16","doi-asserted-by":"publisher","first-page":"1256","DOI":"10.1016\/j.ttbdis.2016.07.004","volume":"7","author":"T Bouzouraa","year":"2016","unstructured":"Bouzouraa T, Rene-Martellet M, Chene J, Attipa C, Lebert I, Chalvet-Monfray K, et al. Clinical and laboratory features of canine Anaplasma platys infection in 32 naturally infected dogs in the Mediterranean basin. Ticks Tick-Borne Dis. 2016;7(6):1256\u201364.","journal-title":"Ticks Tick-Borne Dis"},{"key":"2083_CR17","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1186\/1756-3305-7-111","volume":"7","author":"L Solano-Gallego","year":"2014","unstructured":"Solano-Gallego L, Villanueva-Saz S, Carbonell M, Trotta M, Furlanello T, Natale A. Serological diagnosis of canine leishmaniosis: comparison of three commercial ELISA tests (Leiscan, ID screen and Leishmania 96), a rapid test (speed Leish K) and an in-house IFAT. Parasit Vectors. 2014;7:111.","journal-title":"Parasit Vectors"},{"issue":"4","key":"2083_CR18","doi-asserted-by":"publisher","first-page":"281","DOI":"10.1016\/j.vetpar.2009.03.025","volume":"163","author":"SE Shaw","year":"2009","unstructured":"Shaw SE, Langton DA, Hillman TJ. Canine leishmaniosis in the United Kingdom: a zoonotic disease waiting for a vector? Vet Parasitol. 2009;163(4):281\u20135.","journal-title":"Vet Parasitol"},{"key":"2083_CR19","doi-asserted-by":"publisher","first-page":"129","DOI":"10.1016\/j.vetpar.2017.07.033","volume":"244","author":"Saran Davies","year":"2017","unstructured":"Davies S, Abdullah S, Helps C, Tasker S, Newbury H, Wall R. Prevalence of ticks and tick-borne pathogens: Babesia and Borrelia species in ticks infesting cats of Great Britain. Vet Parasitol. 2017;244:129-35.","journal-title":"Veterinary Parasitology"},{"issue":"1-2","key":"2083_CR20","doi-asserted-by":"publisher","first-page":"167","DOI":"10.1016\/j.vetmic.2009.07.006","volume":"140","author":"EN Barker","year":"2010","unstructured":"Barker EN, Tasker S, Day MJ, Warman SM, Woolley K, Birtles R, et al. Development and use of real-time PCR to detect and quantify Mycoplasma haemocanis and \u201cCandidatus mycoplasma haematoparvum\u201d in dogs. Vet Microbiol. 2010;140(1-2):167\u201370.","journal-title":"Vet Microbiol"},{"issue":"6","key":"2083_CR21","doi-asserted-by":"publisher","first-page":"707","DOI":"10.1016\/S0035-9203(00)90243-8","volume":"94","author":"P Parola","year":"2000","unstructured":"Parola P, Roux V, Camicas J-L, Baradji I, Brouqui P, Raoult D. Detection of ehrlichiae in African ticks by polymerase chain reaction. Trans R Soc Trop Med Hyg. 2000;94(6):707\u20138.","journal-title":"Trans R Soc Trop Med Hyg"},{"issue":"1","key":"2083_CR22","doi-asserted-by":"publisher","first-page":"130","DOI":"10.1186\/s13071-017-2063-2","volume":"10","author":"C Attipa","year":"2017","unstructured":"Attipa C, Papasouliotis K, Solano-Gallego L, Baneth G, Nachum-Biala Y, Sarvani E, et al. Prevalence study and risk factor analysis of selected bacterial, protozoal and viral, including vector-borne, pathogens in cats from Cyprus. Parasit Vectors. 2017;10(1):130.","journal-title":"Parasit Vectors"}],"container-title":["BMC Veterinary Research"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1186\/s12917-019-2083-6.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/article\/10.1186\/s12917-019-2083-6\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1186\/s12917-019-2083-6.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,9,16]],"date-time":"2020-09-16T19:13:40Z","timestamp":1600283620000},"score":1,"resource":{"primary":{"URL":"https:\/\/bmcvetres.biomedcentral.com\/articles\/10.1186\/s12917-019-2083-6"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,9,18]]},"references-count":22,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2019,12]]}},"alternative-id":["2083"],"URL":"https:\/\/doi.org\/10.1186\/s12917-019-2083-6","relation":{},"ISSN":["1746-6148"],"issn-type":[{"value":"1746-6148","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,9,18]]},"assertion":[{"value":"9 February 2019","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"6 September 2019","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"18 September 2019","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"This study was ethically approved by the University of Bristol\u2019s Animal Welfare and Ethical Review Board (Veterinary Investigation number: 15\/022) as well as the Royal Veterinary Collage\u2019s Ethics and Welfare Committee (Veterinary Investigation number: 20141292). All procedures were performed in accordance with Cypriot legislation, which does not requires specific ethical approval from a local ethics committee [The Dogs LAW, N. 184 (I)\/2002], following written and informed consent being obtained from all dog owners.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"CML, KP, JB and JSB work for IDEXX laboratories the manufacturer of SNAP\u00ae 4Dx Plus\u00ae test kit.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"331"}}